Prostate Cancer Patient Characteristics Associated With a Strong Preference to Preserve Sexual Function and Receipt of Active Surveillance

JNCI: Journal of the National Cancer Institute, Apr 2018

Men with early-stage prostate cancer have multiple options that have similar oncologic efficacy but vary in terms of their impact on quality of life. In low-risk cancer, active surveillance is the option that best preserves patients’ sexual function, but it is unknown if patient preference affects treatment selection. Our objectives were to identify patient characteristics associated with a strong preference to preserve sexual function and to determine whether patient preference and baseline sexual function level are associated with receipt of active surveillance in low-risk cancer.

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Prostate Cancer Patient Characteristics Associated With a Strong Preference to Preserve Sexual Function and Receipt of Active Surveillance

JNCI J Natl Cancer Inst ( Prostate Cancer Patient Characteristics Associated With a Strong Preference to Preserve Sexual Function and Receipt of Active Surveillance James R. Broughman 0 1 Ramsankar Basak 0 1 Matthew E. Nielsen 0 1 Bryce B. Reeve 0 1 Deborah S. Usinger 0 1 Kiayni C. Spearman 0 1 Paul A. Godley 0 1 Ronald C. Chen 0 1 0 The Author 2017. Published by Oxford University Press. All rights reserved. For Permissions , please 1 Affiliations of authors: Department of Radiation Oncology (JRB , RB, DSU, KCS, RCC) , School of Medicine (JRB, BBR, PAG, RCC), Lineberger Comprehensive Cancer Center (PAG, RCC), Department of Urology (MEN), and Gillings School of Global Public Health (BBR), University of North Carolina at Chapel Hill , Chapel Hill, NC , USA Background: Men with early-stage prostate cancer have multiple options that have similar oncologic efficacy but vary in terms of their impact on quality of life. In low-risk cancer, active surveillance is the option that best preserves patients' sexual function, but it is unknown if patient preference affects treatment selection. Our objectives were to identify patient characteristics associated with a strong preference to preserve sexual function and to determine whether patient preference and baseline sexual function level are associated with receipt of active surveillance in low-risk cancer. Methods: In this population-based cohort of men with localized prostate cancer, baseline patient-reported sexual function was assessed using a validated instrument. Patients were also asked whether preservation of sexual function was very, somewhat, or not important. Prostate cancer disease characteristics and treatments received were abstracted from medical records. A modified Poisson regression model with robust standard errors was used to compute adjusted risk ratio (aRR) estimates. All statistical tests were two-sided. Results: Among 1194 men, 52.6% indicated a strong preference for preserving sexual function. Older men were less likely to have a strong preference (aRR ¼ 0.98 per year, 95% confidence interval [CI] ¼ 0.97 to 0.99), while men with normal sexual function were more likely (vs poor function, aRR ¼ 1.59, 95% CI ¼ 1.39 to 1.82). Among 568 men with low-risk cancer, there was no clear association between baseline sexual function or strong preference to preserve function with receipt of active surveillance. However, strong preference may differnetially impact those with intermediate baseline function vs poor function (Pinteraction ¼ .02). Conclusions: Treatment choice may not always align with patients' preferences. These findings demonstrate opportunities to improve delivery of patient-centered care in early prostate cancer. - Prostate cancer is the most common nonskin cancer among men, with more than 180 000 new cases diagnosed each year in the United States ( 1 ). Over 90% of newly diagnosed patients have localized disease and are potentially curable ( 2,3 ). These patients often have several treatment options available—which can include active surveillance, radical prostatectomy, or radiation therapy—which have been shown to result in similar survival (4) but different quality of life effects in terms of sexual, urinary, and bowel function ( 5–13 ). Radical prostatectomy is associated with worse sexual function and urinary incontinence compared with active surveillance, external beam radiotherapy and brachytherapy with worse short-term urinary obstruction and irritation, and external beam radiotherapy with worse short-term bowel symptoms ( 14 ). Therefore, it is well recognized that treatment decisions for localized prostate cancer are preference-sensitive and need to account for each patient’s goals and priorities ( 15,16 ). Specifically, different treatment options can have different magnitudes of impact on a patient’s sexual function ( 13,14,17 ). For many men diagnosed with localized prostate cancer, choosing a treatment option that better allows preservation of sexual function may be prioritized. On the other hand, as the median age of prostate cancer diagnosis is 66 years ( 1 ), some men may already have clinically significant baseline sexual dysfunction, and function preservation may not be a high priority. It seems logical that part of the treatment decision-making process between the patient and his physicians would be consideration of his baseline sexual function level and the relative priority he places on preserving this function. For men with low-risk prostate cancer that is unlikely to be life threatening, active surveillance is the best option to preserve sexual function. In a population-based, sociodemographically diverse, prospective cohort of newly diagnosed prostate cancer patients, baseline (pretreatment) sexual function was assessed using a validated quality of life instrument, and each patient also indicated whether preserving sexual function was of high priority. In this study, we sought to examine patient characteristics (including age, race, marital status, baseline sexual function, and prostate cancer aggressiveness) associated with a high priority for preserving sexual function. In addition, in low-risk patients, we examined whether baseline sexual functional level and patient preference were associated with receipt of active surveillance—to empirically assess whether these factors impacted treatment decisions. Methods Patient Population The North Carolina Prostate Cancer Comparative Effectiveness and Survivorship Study (NC ProCESS) is a population-based cohort of prostate cancer patients, enrolled prior to treatment and followed prospectively. This study was approved by the University of North Carolina institutional review board. Details of patient identification and enrollment were described previously ( 18 ), and all patients provided written informed consent. Briefly, patients with newly diagnosed prostate cancer were identified through Rapid Case Ascertainment of the North Carolina Central Cancer Registry from all North Carolina counties between 2011 and 2013. Upon identification, the patient was mailed an introductory letter describing the study. This was followed by a phone call from the study team; if a patient agreed to participate, a baseline survey was conducted at the same time (detailed below). The median time from date of diagnosis to study enrollment and baseline survey was five weeks (range ¼ 3.1–18.9 weeks). Patients who had already initiated any prostate cancer treatment were ineligible. Among all eligible participants, 57.4% agree to participate and were enrolled. Data Collection A baseline/pretreatment survey was conducted prior to treatment for all enrolled patients. Demographic information was collected by patient report and included date of birth, race, marital status, educational attainment, and health insurance. Baseline sexual function was assessed using the validated Prostate Cancer Symptom Indices (PCSI) ( 5,6,17,19–21 ). The Sexual Dysfunction domain of the PCSI includes five questions that assess patient erectile function (firmness, difficulty getting and keeping erections), ejaculation, and orgasm. Answers to these questions are transformed to an overall scale score from 0 (no dysfunction) to 100 (maximum dysfunction). In addition to a numerical score, the PCSI has also previously validated categorizing patients into three levels of function: normal, intermediate, or poor ( 6,17 ). As defined by the instrument, normal function describes a patient with essentially no sexual dysfunction or distress. Intermediate function describes patients with abnormal but useful sexual function ( 6 ). Patients with poor sexual function have no useful function or have had no sexual activity within the past four weeks. In addition, patients were asked the question “Preserving your ability to have sex. Would you say this is. . .” And response choices were very important, somewhat important, or not important. For purposes of data analysis, we considered patients who responded “very important” to have a strong preference for preserving sexual function, and those who indicated “somewhat” or “not important” to have a lower preference for function preservation. Prostate cancer diagnosis information (prostate-specific antigen [PSA] level, Gleason score, and clinical stage) and first course of treatment received within one year of diagnosis were abstracted from medical records. Only patients with early-stage (nonmetastatic) prostate cancer were included for analysis. Patients who pursued initial active surveillance but subsequently received treatment were counted as “active surveillance,” as were patients who did not receive any treatment within one year of diagnosis. Prostate cancer risk group was categorized using definitions from the National Comprehensive Cancer Network (NCCN) ( 22 ). Statistical Analysis In comparing patient characteristics between groups, P values were calculated using t tests for continuous variables and the chi-square test for categorical variables. One goal of this study was to examine characteristics associated with patients who indicated a strong preference to preserve sexual function in their treatment decision-making. We compared the baseline sexual function scores of patients who indicated strong preference vs lower preference for preserving sexual function. In addition, multivariable regression was used to examine additional factors associated with a strong preference for sexual function preservation. Covariates examined included baseline sexual function level, age, marital status, race, NCCN risk group, and education. Specifically, a modified Poisson regression model with robust standard errors was used to compute adjusted risk ratio (aRR) estimates. Another study goal was to empirically assess whether patient preference impacted treatment received. Specifically, in low-risk prostate cancer patients, active surveillance is a standard option and best preserves sexual function ( 23 ). Therefore, we hypothesized that low-risk patients with a strong preference for preserving function and those with normal baseline sexual function would be most likely to receive active surveillance. Stratifying patients into six groups based on baseline sexual function level (normal, intermediate, poor) and patient preference to preserve function (strong preference vs lower preference), we examined whether the use of active surveillance differed by group. Our hypothesis was formally tested using multivariable modified Poisson regression analysis, which E L C I T R A Importance of preserving sexual function Strong preference (n ¼ 628) Lower preference (n ¼ 566) *P values were calculated using t tests for continuous variables and the chi-square test for categorical variables. All P values were two-sided. NCCN ¼ National Comprehensive Cancer Network; VA ¼ Veterans Affairs. examined whether patient preference and baseline sexual function level were associated with receipt of active surveillance, and aRR was reported; a preference*baseline function term specifically examined whether there is an interaction effect between these two variables. Other covariates included marital status, age, and race. All statistical analysis was performed using SAS version 9.4 (Cary, NC), and a P value of less than .05 was considered statistically significant. All statistical tests were two-sided. Results Patient Characteristics and Preference for Preservation of Sexual Function This population-based cohort of 1194 patients is sociodemographically diverse, with 27.9% overall being nonwhite and 32.1% with high school or less education. A total of 628 men (52.6%) indicated a strong preference for preserving sexual function, and 566 patients (47.4%) indicated a lower preference (Table 1). Patients who indicated a strong preference for sexual function preservation had statistically significantly better baseline function (sexual dysfunction score, mean ¼ 34.5, SD ¼ 35.4) than patients who indicated a lower preference for function preservation (mean ¼ 53.5, SD ¼ 39.5, P < .001) (Table 1). In addition, examining baseline sexual functional levels in the two patient groups revealed a more nuanced picture. Among patients who indicated a strong preference to preserve sexual function, 36.4% had normal baseline function but 34.1% actually had poor function. Conversely, 20.6% of patients who indicated a lower preference for function preservation had normal baseline function. Multivariable analysis confirmed the finding that poor baseline sexual function was associated with lower likelihood of patients indicating a strong preference for function preservation (normal vs poor sexual function aRR ¼ 1.59, 95% CI ¼ 1.39 to 1.82) (Table 2). Older patients were also less likely to indicate a strong preference to preserve sexual function (aRR ¼ 0.98 per year, P < .001), as were white patients (aRR ¼ 0.68 to 0.86, P < .001) and men with high-risk prostate cancer (compared with low-risk prostate cancer; aRR ¼ 0.71 to 1.00, P ¼ .06). Results specifically for the low-risk patient subgroup were similar (Supplementary Tables 1 and 2, available online). Sensitivity analysis recategorizing patients as “very important” and “somewhat important” vs “not important” also showed age and baseline sexual function to be statistically significantly associated with a stronger preference to preserve function (Supplementary Tables 3 and 4, available online). Treatment Patterns Table 3 summarizes the treatment patterns of 568 patients with low-risk prostate cancer, stratified by baseline sexual function level and preference for function preservation. Overall, 43.4% of low-risk patients received active surveillance. However, we found no evidence to support our hypothesis of a higher use of active surveillance in patients with a strong preference to preserve their sexual function. Among patients with normal baseline sexual function and a strong preference to preserve this function, 39.2% received active surveillance; the proportion of patients who received active surveillance was actually higher 67 (41-81) 262 (47.2) 207 (37.3) 86 (15.5) for patients who had normal baseline sexual function but indicated lower preference to preserve function (49.2%). A similar finding was seen for patients with poor baseline sexual function, where again a numerically higher proportion of patients who indicated a lower preference to preserve sexual function received active surveillance. We formally tested our hypothesis using multivariable analysis, examining factors associated with active surveillance in low-risk patients (Table 4). Older patients were statistically significantly more likely to undergo active surveillance (aRR ¼ 1.02 to 1.06 per year, P < .001). Interaction terms examined whether patient preference differentially impacted patients with different baseline sexual function levels in their “risk” of receiving active surveillance. Results suggest that patients with a strong preference to preserve sexual function are more likely to receive active surveillance if they have intermediate baseline function than poor baseline function (Pinteraction ¼ .02). However, preference to preserve sexual function did not differentially impact patients with baseline normal vs those with poor function. Discussion In this population-based and diverse cohort of men with localized prostate cancer, we report several notable findings that add to the published literature. First, more than half of patients with newly diagnosed prostate cancer had a strong preference to preserve sexual function. Second, not surprisingly, younger patients and those with better baseline sexual function were more likely to indicate a strong preference for preserving sexual function. Third, while 43% of low-risk patients received active surveillance, there was not a clear pattern of patient’s baseline function or preference for sexual function preservation being associated with receipt of active surveillance. To the best of our knowledge, this study is the first to assess whether patient preference for sexual function preservation matched treatment received in a large, population-based and diverse cohort of prostate cancer patients. Prior studies ( 24–27 ) along with ours provide insights into the prostate cancer treatment-making process. Prostate cancer is unique in that many patients with localized disease have multiple options that have similar oncologic efficacy but differ in terms of their impact on quality of life ( 5–13 ). Thus, decision-making for men with early prostate cancer is a preference-sensitive process and should take into account a patient’s priorities. For low-risk patients, active surveillance results in similar overall survival compared with radiation and surgery and better preserves sexual function ( 4,23 ). In light of this, physicians should inform their low-risk patients that active surveillance would best meet their preference for preserving sexual function without compromising life expectancy. However, it is unknown whether patient preference is elicited by their physicians or taken into account in final treatment selection. With this background, there are several findings that warrant further discussion. First, while we found that better baseline sexual function was associated with a higher likelihood of men indicating a strong preference for function preservation, there are important exceptions. As Table 1 detailed, one-third of men with normal baseline sexual function indicated a lower preference for functional preservation, while 40% of men with poor baseline function indicated a strong preference. This finding suggests that simply ascertaining a patient’s baseline sexual function level is insufficient for determining patient treatment goals because physicians cannot assume that patients with good sexual function will always place a high priority on preserving this function. To allow patients to make an informed decision on treatment, physicians need to directly ask patients about their priorities during the decision-making process, including preferences for sexual function, other quality-of-life impacts (eg, urinary function), and aggressiveness of cancer treatment. Our multivariable analysis showed that additional factors associated with patient preference included patient age and cancer aggressiveness. This study also showed a disconnect between patients’ preference for sexual function preservation and treatment received. One possible explanation is that physicians may not routinely elicit patient preferences in making treatment recommendations ( 28–30 ). Prior studies have shown that prostate cancer treatment decisions are associated with physician specialty *ADT ¼ androgen deprivation therapy; AS ¼ active surveillance; NCCN ¼ National Comprehensive Cancer Network; RP ¼ radical prostatectomy; RT ¼ radiotherapy (includes external beam radiotherapy and brachytherapy). E L C I T R A ( 31,32 ), and patients who are younger and healthier are more likely to receive surgery, while older patients more likely to receive radiotherapy or no treatment. Our findings are consistent with this and showed that older age was statistically significantly associated with active surveillance. Whereas age is a factor that is relatively easy to ascertain during a clinic visit, thoroughly assessing patients’ baseline sexual function level and preferences is more time consuming, and there may also be other cultural barriers to accurately attaining this information in the clinical setting. The development and use of decision aids in prostate cancer can help systematically clarify patient priorities as well as educate patients about treatments that align with their goals. Several analyses found that decision aids increase patient knowledge and involvement throughout the decisionmaking process (33), thus facilitating the delivery of highquality, patient-centered care. Indeed, patient knowledge about active surveillance and being fully informed about expectations are important factors in patient treatment selection ( 34 ). This study has several strengths and potential limitations. A strength is the population-based design of modern patients, which yielded a cohort that is sociodemographically diverse and more representative than institutional reports. However, this study was conducted in one East Coast state and may not be representative of other states or regions, and the 57% response rate in this study could further limit the generalizability of results. This study is also unique in assessing patientreported sexual function prior to treatment, as well as patients’ preference to preserve this function. We are unware of other large population-based cohorts that contain this information. However, the latter question was created specifically for this study, as no validated assessment was available in the published literature. Furthermore we did not quantify patients’ preferences or their understanding of their preferences directly—and therefore a definitive conclusion about lack of congurency in patient preferences with treatment selection cannot be made. It is also possible that the expressed preference for maintaining sexual function captured in this study could reflect physician-patient interaction about treatment options and consequences. Another potential limitation is that while a patient may have indicated a strong preference to preserve sexual function, he may have an even stronger desire for aggressive treatment or have anxiety related to active surveillance, and we did not capture the latter information in this study. However, low-risk prostate cancer is unlikely to be life threatening. For patients with these early diagnoses who express concurrent preferences regarding maximizing survival and preserving sexual function, and if indeed these preferences were ascertained by their physicians, informed decision-making should include clarification that choosing active surviellance would be concordant with patient preferences without compromising survival outcomes. Finally, this study did not survey physicians, so we assessed the patients’ treatment selection but were unable to directly make conclusions about physician recommendations. The physician plays an important role in treatment selection, and recommendations vary considerably by specialty ( 32 ). Furthermore, certain specialties may be more or less attentive to the preferences of their patients for the preservation of sexual function. In this population-based cohort of 1194 men with newly diagnosed localized prostate cancer, more than half (52.6%) indicated a strong preference to preserve sexual function in their treatment decision-making process. However, among men with a low-risk diagnosis, there was no clear association between patient preference or baseline sexual function level with receipt of active surveillance. Although many men with low-risk disease report that preserving sexual function is a high priority, many do not receive active surveillance, which is the treatment most aligned with this preference. These findings call for improved efforts for delivering high-quality, patient-centered care in this common disease. Funding Notes This study was funded by a Patient-Centered Outcomes Research Institute (PCORI) contract CER-1310-06453 and a contract from the Agency for Healthcare Research and Quality (HHSA290-2005-0040-I-TO6) to PI Ronald Chen. The sponsors were not involved with the collection, management, analysis, or interpretation of the data; preparation, review, or approval of the manuscript; or the decision to submit the manuscript for publication. There are no conflicts of interest related to this study. Dr. Chen reports receiving grants and personal fees from Accuray and personal fees from Astellas and Medivation. 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Broughman, James R, Basak, Ramsankar, Nielsen, Matthew E, Reeve, Bryce B, Usinger, Deborah S, Spearman, Kiayni C, Godley, Paul A, Chen, Ronald C. Prostate Cancer Patient Characteristics Associated With a Strong Preference to Preserve Sexual Function and Receipt of Active Surveillance, JNCI: Journal of the National Cancer Institute, 2018, 420-425, DOI: 10.1093/jnci/djx218